Subtoxic product levels limit the epoxidation capacity of recombinant E. coli by increasing microbial energy demands

Journal of Biotechnology

Volumn 163, Issue 2, 2013, Pages 194-203

  Kuhn, Daniel ^a   Fritzsch, Frederik S O ^a   Zhang, Xiumei ^a   Wendisch, Volker F ^b   Blank, Lars M ^a,c   Bühler, Bruno ^a   Schmid, Andreas ^a  

^a TU DORTMUND UNIVERSITY   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Cofactor regeneration; Metabolic engineering; Metabolic flux analysis; Styrene monooxygenase; Two liquid phase biotransformation; Whole cell redox biocatalysis

Indexed keywords

BIOCATALYSIS; COFACTOR REGENERATION; METABOLIC FLUX ANALYSIS; MONOOXYGENASES; TWO-LIQUID PHASE BIOTRANSFORMATION;

BIOCATALYSTS; CULTIVATION; ESCHERICHIA COLI; KNOWLEDGE BASED SYSTEMS; LIQUIDS; METABOLIC ENGINEERING; STYRENE;

METABOLISM;

ACETIC ACID; GLUCOSE; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; RECOMBINANT ENZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STYRENE; STYRENE OXIDE; STYRENE OXYGENASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

AEROBIC METABOLISM; ARTICLE; ASYMMETRIC CATALYSIS; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM MUTANT; BACTERIUM TRANSFORMATION; BIOCATALYSIS; BIOCATALYST; BIOMASS; CATALYST SUPPORT; CITRIC ACID CYCLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENERGY METABOLISM; EPOXIDATION; ESCHERICHIA COLI; GROWTH RATE; LIQUID; METABOLIC ENGINEERING; METABOLIC PARAMETERS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROCESS DESIGN; STEADY STATE;

BIOREACTORS; BIOTECHNOLOGY; BIOTRANSFORMATION; ENERGY METABOLISM; EPOXY COMPOUNDS; ESCHERICHIA COLI; GLUCOSE; KINETICS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; NAD; NADP; OXIDATION-REDUCTION; OXYGENASES; RECOMBINANT PROTEINS; SYSTEMS BIOLOGY;

ESCHERICHIA COLI;

EID: 84872188267     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2012.07.194     Document Type: Article

References (58)

1. Alexeeva S., Hellingwerf K.J., de Mattos M.J.T. Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. Journal of Bacteriology 2003, 185:204-209.
2. Aono R., Kobayashi H. Cell surface properties of organic solvent-tolerant mutants of Escherichia coli K-12. Applied and Environment Microbiology 1997, 63:3637-3642.
3. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology 2006, 2:2006.0008.
4. Bekker M., Alexeeva S., Laan W., Sawers G., de Mattos J.T., Hellingwerf K. The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. Journal of Bacteriology 2010, 192:746-754.
5. Bertani G. Studies on lysogenesis I. The mode of phage liberation by lysogenic Escherichia coli. Journal of Bacteriology 1951, 62:293-300.
6. Blank L.M., Ebert B.E., Bühler B., Schmid A. Metabolic capacity estimation of Escherichia coli as platform for redox biocatalysis: constraint based modeling and experimental verification. Biotechnology and Bioengineering 2008, 100:1050-1065.
7. Blank L.M., Ebert B.E., Bühler K., Bühler B. Redox biocatalysis and metabolism: molecular mechanisms and metabolic network analysis. Antioxidants and Redox Signalling 2010, 13:349-394.
8. 13C-flux analysis reveals mechanistic principles of metabolic network robustness to null mutations in yeast. Genome Biology 2005, 6:R49.
9. Blattner F.R., Plunkett G., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453-1462.
10. Bühler B., Blank L.M., Ebert B.E., Bühler K., Schmid A. Energy and cofactor issues in fermentation and oxyfunctionalization processes. The Metabolic Pathway Engineering Handbook: Tools and Applications 2010, CRC Press, Boca Raton, FL, USA, 21_1-21_32. 1st ed. C. Smolke (Ed.).
11. Bühler B., Park J.B., Blank L.M., Schmid A. NADH availability limits asymmetric biocatalytic epoxidation in a growing recombinant Escherichia coli strain. Applied and Environment Microbiology 2008, 74:1436-1446.
12. Bühler B., Schmid A. Process implementation aspects for biocatalytic hydrocarbon oxyfunctionalization. Journal of Biotechnology 2004, 113:183-210.
13. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 1995, 158:9-14.
14. Emmerling M., Dauner M., Ponti A., Fiaux J., Hochuli M., Szyperski T., Wüthrich K., Bailey J.E., Sauer U. Metabolic flux responses to pyruvate kinase knockout in Escherichia coli. Journal of Bacteriology 2002, 184:152-164.
15. Fischer E., Sauer U. Metabolic flux profiling of Escherichia coli mutants in central carbon metabolism using GC-MS. European Journal of Biochemistry 2003, 270:880-891.
16. Fuhrer T., Fischer E., Sauer U. Experimental identification and quantification of glucose metabolism in seven bacterial species. Journal of Bacteriology 2005, 187:1581-1590.
17. Georgellis D., Kwon O., Lin E.C.C. Quinones as the redox signal for the Arc two-component system of bacteria. Science 2001, 292:2314-2316.
18. Heipieper H.J., Neumann G., Cornelissen S., Meinhardt F. Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Applied Microbiology and Biotechnology 2007, 74:961-973.
19. Heyland J., Fu J.A., Blank L.M. Correlation between TCA cycle flux and glucose uptake rate during respiro-fermentative growth of Saccharomyces cerevisiae. Microbiology 2009, 155:3827-3837.
20. Ishii N., Nakahigashi K., Baba T., Robert M., Soga T., Kanai A., Hirasawa T., Naba M., Hirai K., Hoque A., Ho P.Y., Kakazu Y., Sugawara K., Igarashi S., Harada S., Masuda T., Sugiyama N., Togashi T., Hasegawa M., Takai Y., Yugi K., Arakawa K., Iwata N., Toya Y., Nakayama Y., Nishioka T., Shimizu K., Mori H., Tomita M. Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 2007, 316:593-597.
21. Jackson J.B. Proton translocation by transhydrogenase. FEBS Letters 2003, 545:18-24.
22. Julsing M.K., Kuhn D., Schmid A., Bühler B. Resting cells of recombinant E. coli show high epoxidation yields on energy source and high sensitivity to product inhibition. Biotechnology and Bioengineering 2012, 109:1109-1119.
23. Kitano H. Systems biology: a brief overview. Science 2002, 295:1662-1664.
24. Koebmann B.J., Westerhoff H.V., Snoep J.L., Nilsson D., Jensen P.R. The glycolytic flux in Escherichia coli is controlled by the demand for ATP. Journal of Bacteriology 2002, 184:3909-3916.
25. Kuhn D., Blank L.M., Schmid A., Bühler B. Systems biotechnology: rational whole-cell biocatalyst and bioprocess design. Engineering in Life Sciences 2010, 10:384-397.
26. Kuhn D., Julsing M.K., Heinzle E., Bühler B. Systematic optimization of a biocatalytic two-liquid phase oxyfunctionalization process guided by ecological and economic assessment. Green Chemistry 2012, 14:645-653.
27. Kuhn D., Kholiq M.A., Heinzle E., Bühler B., Schmid A. Intensification and economic and ecological assessment of a biocatalytic oxyfunctionalization process. Green Chemistry 2010, 12:815-827.
28. Majewski R.A., Domach M.M. Simple constrained optimization view of acetate overflow in Escherichia coli. Biotechnology and Bioengineering 1990, 35:732-738.
29. Messing J. A multi-purpose cloning system based on the single stranded bacteriophage M13. Recombinant DNA Technical Bulletin 1979, 79-99:43-48.
30. 13C-experiments and gas chromatography-mass spectrometry data - protocol and principles. Metabolomics - Methods and Protocols 2006, 171-197. Humana Press Inc., Tetowa, NJ, USA. W. Weckwerth (Ed.).
31. Nanchen A., Schicker A., Sauer U. Nonlinear dependency of intracellular fluxes on growth rate in miniaturized continuous cultures of Escherichia coli. Applied and Environment Microbiology 2006, 72:1164-1172.
32. Nizam S.A., Zhu J.F., Ho P.Y., Shimizu K. Effects of arcA and arcB genes knockout on the metabolism in Escherichia coli under aerobic condition. Biochemical Engineering Journal 2009, 44:240-250.
33. Otero J.M., Nielsen J. Industrial systems biology. Biotechnology and Bioengineering 2010, 105:439-460.
34. Otto K., Hofstetter K., Röthlisberger M., Witholt B., Schmid A. Biochemical characterization of StyAB from Pseudomonas sp strain VLB120 as a two-component flavin-diffusible monooxygenase. Journal of Bacteriology 2004, 186:5292-5302.
35. Panke S., de Lorenzo V., Kaiser A., Witholt B., Wubbolts M.G. Engineering of a stable whole-cell biocatalyst capable of (S)-styrene oxide formation for continuous two-liquid-phase applications. Applied and Environment Microbiology 1999, 65:5619-5623.
36. Panke S., Held M., Wubbolts M.G., Witholt B., Schmid A. Pilot-scale production of (S)-styrene oxide from styrene by recombinant Escherichia coli synthesizing styrene monooxygenase. Biotechnology and Bioengineering 2002, 80:33-41.
37. Panke S., Meyer A., Huber C.M., Witholt B., Wubbolts M.G. An alkane-responsive expression system for the production of fine chemicals. Applied and Environment Microbiology 1999, 65:2324-2332.
38. Panke S., Witholt B., Schmid A., Wubbolts M.G. Towards a biocatalyst for (S)-styrene oxide production: characterization of the styrene degradation pathway of Pseudomonas sp strain VLB120. Applied and Environment Microbiology 1998, 64:2032-2043.
39. Panke S., Wubbolts M.G., Schmid A., Witholt B. Production of enantiopure styrene oxide by recombinant Escherichia coli synthesizing a two-component styrene monooxygenase. Biotechnology and Bioengineering 2000, 69:91-100.
40. Park J.B., Bühler B., Habicher T., Hauer B., Panke S., Witholt B., Schmid A. The efficiency of recombinant Escherichia coli as biocatalyst for stereospecific epoxidation. Biotechnology and Bioengineering 2006, 95:501-512.
41. Park J.B., Bühler B., Panke S., Witholt B., Schmid A. Carbon metabolism and product inhibition determine the epoxidation efficiency of solvent-tolerant Pseudomonas sp. strain VLB120ΔC. Biotechnology and Bioengineering 2007, 98:1219-1229.
42. Perrenoud A., Sauer U. Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli. Journal of Bacteriology 2005, 187:3171-3179.
43. Ruinatscha R., Dusny C., Bühler K., Schmid A. Productive asymmetric styrene epoxidation based on a next generation electroenzymatic methodology. Advanced Synthesis and Catalysis 2009, 351:2505-2515.
44. Sambrook J., Russell D.W. Molecular cloning - A laboratory manual 2001, Cold Spring Harbor Laboratory Press, New York, NY, USA. 3rd ed.
45. 13C-based flux analysis. Molecular Systems Biology 2006, 2:62.
46. Sauer U., Canonaco F., Heri S., Perrenoud A., Fischer E. The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. Journal of Biological Chemistry 2004, 279:6613-6619.
47. Sauer U., Lasko D.R., Fiaux J., Hochuli M., Glaser R., Szyperski T., Wüthrich K., Bailey J.E. Metabolic flux ratio analysis of genetic and environmental modulations of Escherichia coli central carbon metabolism. Journal of Bacteriology 1999, 181:6679-6688.
48. Shimizu K. Toward systematic metabolic engineering based on the analysis of metabolic regulation by the integration of different levels of information. Biochemical Engineering Journal 2009, 46:235-251.
49. Sikkema J., de Bont J.A.M., Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews 1995, 59:201-222.
50. Stephanopoulos G., Alper H., Moxley J. Exploiting biological complexity for strain improvement through systems biology. Nature Biotechnology 2004, 22:1261-1267.
51. van Beilen J.B., Duetz W.A., Schmid A., Witholt B. Practical issues in the application of oxygenases. Trends in Biotechnology 2003, 21:170-177.
52. van Winden W.A., Wittmann C., Heinzle E., Heijnen J.J. Correcting mass isotopomer distributions for naturally occurring isotopes. Biotechnology and Bioengineering 2002, 80:477-479.
53. Veit A., Polen T., Wendisch V.F. Global gene expression analysis of glucose overflow metabolism in Escherichia coli and reduction of aerobic acetate formation. Applied Microbiology and Biotechnology 2007, 74:406-421.
54. Vemuri G.N., Altman E., Sangurdekar D.P., Khodursky A.B., Eiteman M.A. Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Applied and Environment Microbiology 2006, 72:3653-3661.
55. 13C metabolic flux analysis. Metabolic Engineering 2001, 3:195-206.
56. Wittmann C. Fluxome analysis using GC-MS. Microbial Cell Factories 2007, 6:6.
57. Woodley J.M. Choice of biocatalyst form for scalable processes. Biochemical Society Transactions 2006, 34:301-303.
58. 13C-glucose experiments. BMC Bioinformatics 2005, 6:209.